On the trail of the Black Death

A third of Europe's population died over four years due to the Black Death. But was it really spread by rats and fleas? Could it have been caused by a virus? And what has that got to do with the modern-day spread of HIV?

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In the old days...

For hundreds of thousand of years, mankind's basic economic unit was the tribe. Each tribe wandered the landscape hunting and gathering. There was very little contact with members of other tribes. This didn't make things easy for micro-organisms that cause disease.

If a virulent organisms appeared on the scene — a mutation from an earlier mild form of an illness, or one that made the jump from an animal to infect humans — there was nowhere much for it to go. It made the members of the tribe very sick, or maybe killed them, and that was it.

Then about ten thousand years ago, people began to settle down in the fertile river valleys of the Levant, Egypt and India, cultivating crops and raising livestock. Settlements grew into cities which became empires.

It was godsend for micro-organisms. Now they could spread much further and infect far more people. As trade routes opened up, sudden and devastating pestilences originating in Africa and the Levant swept into Greek and Roman worlds, devastating populations, destroying armies and changing the course of history.

But the deadliest of all arrived when the trade routes opened to the East. In the 13th century, trade between Europe and China took off, thanks to the open border polices of the Mongols and the insatiable demand by Europeans for perfumes of Arabia, the silks of China, and the spices of India.

The Black Death arrives

In 1334 in the north-eastern Chinese province of Hopei, China, a new disease appeared. Highly virulent, highly infectious, it killed about 90 percent of the population — some 5,000,000 people. It then made its way west, striking India, Syria, and Mesopotamia.

In 1346, it struck a Genoese trading station Kaffa on the Crimean Peninsula of the Black Sea - right between the empires of Islam and Christianity. Kaffa was under siege from the Muslim Tartar forces and its inhabitants were starving. Suddenly though, the Tartars started dropping like flies. The Black Death had arrived.

But there was little comfort for the besieged Genoese. Before retreating, the commander of the Tartars catapulted a few plague infested corpses over the city walls. Hoping to escape, the Genoese sailed away in four ships. But by the time they reached Messina, Sicily, most of those on board were already dead. The ships were ordered out of the harbour - but too late. The Great Pestilence, as it would come to be known, had reached Europe.

Here's a description from a Giovanni Boccaccio, who was there when it struck his home town of Florence in 1348:-

"... it began with swellings in the groin and armpit, in both men and women, some of which were as big as apples and some of which were shaped like eggs, some were small and others were large; the common people called these swellings gavoccioli. From these two parts of the body, the fatal gavaccioli would begin to spread and within a short while would appear over the entire body in various spots; the disease at this point began to take on the qualities of a deadly sickness, and the body would be covered with dark and livid spots, which would appear in great numbers on the arms, the thighs, and other parts of the body; some were large and widely spaced while some were small and bunched together. And just like the gavaciolli earlier, these were certain indications of coming death."

Boccaccio was one of the few who didn't do too badly out of the plague — it gave him the idea for a book. In 1350 he wrote the Decameron, a saucy collection of tales set in a country house where a group of nobles fled to escape the pestilence.

A time of fear and panic

For Europe, the Great Pestilence was a disaster. It spread rapidly, about two miles a day, along the ports of the Mediterranean to Spain, overland across the Alps and the Pyrenees into France and Germany, north to Scandinavia and across the North Sea to Britain and Ireland and as far as Iceland and Greenland.

Families fled, leaving sick relatives to fend for themselves. Law and order barely existed and essential services collapsed. Doctors could do nothing.

The rich fled into the countryside, but the pestilence followed them. Some towns ordered that infected houses be walled up, leaving the inhabitants inside to die. Others banned anyone from entering or leaving the city/town/village — these quarantine measures seemed to limit the spread.

From 1348 to 1352, twenty-five million people died — a third of the population of Europe.

Divine Intervention?

Was it a punishment from God? Anything that catastrophic had to be, religious authorities thought. Bands of hooded men, called flagellators, wearing white robes marked front and back with a red cross, roamed Europe, whipping themselves in ritual public ceremonies. Singing hymns and sobbing, the men beat themselves with scourges studded with iron spikes. Others blamed the Jews for poisoning Christian wells. Still others thought it was due to foul vapours in the air.

Over the next three hundred years, the plague advanced and retreated, advanced and retreated, each time getting less virulent. The last great epidemic was in 1670. Then, mysteriously, it disappeared.

What caused it?

Usually the cause of the Black Death is attributed to Bubonic plague — a disease of rats transmitted to humans by fleas. The fleas bite infected rats and then bite humans, infecting them in turn. The flea is xenopsylla cheopis, the oriental flea, which feeds on the blood of mice, rats (especially the black rat, rattus rattus) guinea pigs, dogs and rabbits. The organism is Yersinia pestis, a rod-shaped bacteria named in honour of Alexander Yersin, a French bacteriologist who successfully isolated the bacteria in Hong Kong in 1894.

In 2001, scientists at the Sanger Centre, Cambridge, UK succeded in mapping the entire genome — the genetic map — of Yersonia for the first time.

They discovered that Yersinia Pestis was originally a harmless bacterium found in the stomach of rats. About 1500 years ago, it worked out how to insert genes from other bacteria and viruses into its genome which allowed it to enter the rat's bloodstream.

This was bad news for the rat and for other hosts, including humans, because it became much more virulent, in other words dangerous. When the flea bit a human, depositing Yersinia into human tissues, the bacteria could travel inside white blood cells to nearby lymph nodes where it could multiply, causing the lymph nodes to swell and suppurate (form pus). It could then escape into the bloodstream and spread to other organs of the body, overwhelming and killing its host in 30 — 50 percent of cases.

Bubonic plague became endemic wherever black rats and fleas lived which was mainly ports and rural villages in temperate climates. As people moved about, it spread. The black rat is a good climber and likes to feed on grain in the cargoes of ships, and that way it travelled to new ports and spread and infected the rat population of a new destination.

So during the Age of Empires and the Middle Ages, as trade advanced, it spread from the Levant to the ports of the Mediterranean. The last wave of epidemics coincided with the invention of the railways and the steam ship around the turn of the century which gave the black rat the chance to find new destinations. Epidemics broke out in California, South America, South Africa, and in 1900, Australia, where it invaded the Rocks area of Sydney and from there spread up and down the east coast. Today it's endemic in parts of Africa and Asia, where, according to the World Health Organisation, it kills about 3000 people each year.

Was Bubonic plague the cause of the Black Death?

The descriptions given by Boccaccio and others didn't seem to fit with what we know about bubonic plague. That was the view of two British researchers, Christopher Duncan and Susan Scott from the University of Liverpool, who in 2001 published a book called Biology of Plagues: Evidence from Historical Populations. In it they pointed out several things that didn't make sense if indeed, the Black Death was caused by bubonic plague. For example;

• How did it spread so quickly? According to written accounts at the time, the Black Death spread on average about 2 miles a day. This implies packs of rats scurrying at breakneck speed across the countryside. But there were no such observations from observers at the time. In fact, eyewitness accounts of the Black Death in towns and villages don't mention rats at all.

• How did it get over the Pyrenees and the Alps? How did it reach Iceland and Greenland? Those are long cold journeys for a plague-ridden rat that prefers warmer climates.

• Why did it spread along trade routes and where crowds of people gathered — in urban centres, at fairs, and amongst armies and processions of people?

• And why was quarantining the only real measure that was effective? Quarantining wouldn't have worked if the plague was spread by rats, because the rats would have escaped from quarantined houses and villages and continued to spread the disease.

Was the Black Death a virus?

There had to be some other means of transmisson than the rat/flea/human pathway. It made much more sense if transmission was from person to person — by an airborne particle — probably a virus, argue Duncan and Scott.

Medieval descriptions of the Black Death — where dark spots appear in the skin — sound more like viral hemorrhagic fever, similar to modern day Ebola, than bubonic plague, they say.

If so, it would explain why it spread so quickly. The virus, they argue, had a long incubation period of about 20 days. During this time — the period between exposure to the virus and getting the symptoms — the person was infectious and spread the disease, unbeknownst to the population.

Here's what they think probably happened. A person — a soldier perhaps or a travelling tradesman who was infected with the Black Death, but wasn't yet ill, arrived in a new town and took up lodgings. That person infected the rest of the household who spread it to other households (usually via visiting children) to the entire village or town. After about two to three weeks the traveller died. Then others fell ill and died. Meanwhile someone from the village had travelled into another village spreading the disease and so on. That's why the disease appeared to travel so fast — two miles a day was the rate at which travellers on average moved across the countryside on foot.

The village of Eyam

It's hard to prove the causative agent was a virus because of course in those days there were no blood tests for viruses. And today it's impossible to extract viral DNA from 700 year-old skeletal remains. But in the last few years some evidence has emerged that seems to support the viral theory.

There may not have been blood tests, but in England at least there were parish records from about 1540. They give a detailed picture of what happened to the inhabitants of even the smallest village — births, deaths, marriages, and baptisms. One such village was Eyam, a lead-mining village in the county of Derbyshire in an area known as the Peak District, in central England.

The Black Death suddenly struck this tiny village in September 1665. The town's rector persuaded the villagers to quarantine themselves to prevent the disease from spreading through the region. During the period of isolation, food was left for the villagers at a well on the parish boundary high up on the hill above the village, and paid for by coins which were dipped in vinegar to disinfect them. It seemed to work, because none of the surrounding areas were affected by the plague. A year later, the first outsiders ventured into Eyam. About half the town had survived.

Genetics to the rescue

In 1996, researchers from the National Institutes of Health in Washington D.C. led by Dr Stephen J O'Brien, tracked down the modern day descendents of Eyam from parish records and tested their DNA. They were curious to know whether the survivors shared any genetic similarity that had helped their ancestors resist the plague. They found high levels of a gene mutation called CCR5-delta 32 amongst the descendents. CCR5 is a gene that codes for a protein on the surface of white blood cells which acts as a receptor for other molecules involved in inflammation

These researchers knew about this protein from previous research on HIV which showed that HIV can slip past the protein, using it as a gateway to get inside and kill white cells. But people who have the mutated form of the gene — CCR5-delta 32 — don't have this protein and their white cells won't allow HIV in. So people with the mutation are resistant to HIV infection — they either don't get HIV at all or are much slower to get it than people who have the normal gene.

Here was the mutation showing up again in the population of Eyam. And not just Eyam. Areas of Europe that had been affected by the plague (including America, which was mostly settled by European plague survivors and their descendents) also had unusually high levels of CCR5-delta 32 — about fourteen per cent of the population compared to two percent in areas that never experienced the Black Death — such as Asia and Africa.

The big jump in the percentage of the population with the mutation has been calculated to have occurred around 700 years ago — around the time of the first major plague epidemic, say Duncan and Scott.

It appears that, beginning 700 years ago, the Black Death increased the genetic frequency of CCR5-delta 32 mutation in the Caucasian gene pool. This protected these populations from later epidemics of both the Black Death and also HIV. The populations of Asia, and Africa had no such protection — and this also explains why HIV/AIDS has spread more quickly there. It also appears that, like HIV, the Black Death was caused by a virus, say Duncan and Scott.

They say that during the period of the Great Pestilence there were probably two separate plagues — a viral haemorrhagic fever in Europe, the Black Death; and a bubonic plague in Asia and parts of the Mediterranean coast caused by Yersinia.

The plague and globalisation

Both epidemics are examples of an evolutionary struggle that has gone on for millions of years between disease causing micro-organisms and hosts. If a micro-organism mutates into a form that makes transmission easier — to a new host for example — then it has the advantage. If the host in turn develops a mutation that protects it from the micro-organism, or develops immunity to it, then it has an advantage over that micro-organism.

The Black Death, dying out in the 17th century, lost the fight. The last great epidemic was in 1670 — after that smallpox took over as the number one infectious disease killer. The Black Death was a victim of its own success. It killed so many of the population so quickly that those left either had genetic resistance or immunity. It had nowhere to go. Bubonic plague was more successful from an evolutionary point of view. It was (and is) deadly too, but it caused sporadic outbreaks in isolated areas, leaving the rest of the population disease free possibly to be infected in future. So bubonic plague survives.

But both epidemics were only possible because of the increased movement of people from place to place. In the Middle Ages, disease could only spread as fast as a person could walk or a ship could sail. In the twenty first century, a new disease could cross the globe by air in twenty-four hours, say Duncan and Scott. Will there another epidemic? Undoubtedly. Will it be as deadly as the Black Death? It's possible. If it happens in the twentieth first century it will travel much faster than two miles a day.